Adaptive evolution of Toll-like receptor 5 in domesticated mammals

BMC Evolutionary Biology

Volumn 12, Issue 1, 2012, Pages

  Smith, Sarah A ^a   Jann, Oliver C ^b   Haig, David ^a   Russell, George C ^c   Werling, Dirk ^d   Glass, Elizabeth J ^b   Emes, Richard D ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c ROYAL VETERINARY COLLEGE   (United Kingdom)

^d MOREDUN RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Adaptive evolution; Cattle; Positive selection; Sheep; SNP; Toll like receptor

Indexed keywords

ADAPTATION; CATTLE; CLADISTICS; DOMESTIC SPECIES; GENE EXPRESSION; LIVESTOCK; MAMMAL; PATHOGEN; POLYMORPHISM; PROTEIN; SHEEP;

BACTERIA (MICROORGANISMS); BOS; MAMMALIA; OVIS ARIES;

FLAGELLIN; TOLL LIKE RECEPTOR 5;

ADAPTATION; ANIMAL; ARTICLE; BACTERIUM; CATTLE; CODON; GENETIC SELECTION; GENETICS; HOST PATHOGEN INTERACTION; LIVESTOCK; MOLECULAR EVOLUTION; PROTEIN DOMAIN; PROTEIN TERTIARY STRUCTURE; SHEEP; SINGLE NUCLEOTIDE POLYMORPHISM;

ADAPTATION, BIOLOGICAL; ANIMALS; BACTERIA; CATTLE; CODON; EVOLUTION, MOLECULAR; FLAGELLIN; HOST-PATHOGEN INTERACTIONS; LIVESTOCK; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; SELECTION, GENETIC; SHEEP; TOLL-LIKE RECEPTOR 5;

EID: 84868007410     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-12-122     Document Type: Article

References (53)

1. Toll-like receptors as molecular switches. Gay NJ, Gangloff M, Weber AN, Nat Rev Immunol 2006 6 693 698 10.1038/nri1916 16917510 (Pubitemid 44298218)
2. Variation matters: TLR structure and species-specific pathogen recognition. Werling D, Jann OC, Offord V, Glass EJ, Coffey TJ, Trends Immunol 2009 30 124 130 10.1016/j.it.2008.12.001 19211304
3. Comparative sequence analysis of leucine-rich repeats (LRRs) within vertebrate toll-like receptors. Matsushima N, Tanaka T, Enkhbayar P, Mikami T, Taga M, Yamada K, Kuroki Y, BMC Genomics 2007 8 124 10.1186/1471-2164-8-124 17517123 (Pubitemid 46995052)
4. Sequence diversity of flagellin (fliC) alleles in pathogenic Escherichia coli. Reid SD, Selander RK, Whittam TS, J Bacteriol 1999 181 153 160 9864325 (Pubitemid 29013666)
5. A history of recurrent positive selection at the toll-like receptor 5 in primates. Wlasiuk G, Khan S, Switzer WM, Nachman MW, Mol Biol Evol 2009 26 937 949 10.1093/molbev/msp018 19179655
6. Signatures of positive selection in Toll-like receptor (TLR) genes in mammals. Areal H, Abrantes J, Esteves PJ, BMC Evol Biol 2011 11 368 10.1186/1471-2148-11-368 22185391
7. A conserved surface on Toll-like receptor 5 recognizes bacterial flagellin. Andersen-Nissen E, Smith KD, Bonneau R, Strong RK, Aderem A, J Exp Med 2007 204 393 403 10.1084/jem.20061400 17283206 (Pubitemid 46294554)
8. Functional characterization of chicken TLR5 reveals species-specific recognition of flagellin. Keestra AM, de Zoete MR, van Aubel RA, van Putten JP, Mol Immunol 2008 45 1298 1307 10.1016/j.molimm.2007.09.013 17964652 (Pubitemid 350299485)
9. Are cattle, sheep, and goats endangered species? Taberlet P, Valentini A, Rezaei HR, Naderi S, Pompanon F, Negrini R, Ajmone-Marsan P, Mol Ecol 2008 17 275 284 10.1111/j.1365-294X.2007.03475.x 17927711 (Pubitemid 350292469)
10. Yang Z, Computational Molecular Evolution Oxford University Press, Oxford 1 2006
11. PAML 4: phylogenetic analysis by maximum likelihood. Yang Z, Mol Biol Evol 2007 24 1586 1591 10.1093/molbev/msm088 17483113 (Pubitemid 47236688)
12. The molecular structure of the Toll-like receptor 3 ligand-binding domain. Bell JK, Botos I, Hall PR, Askins J, Shiloach J, Segal DM, Davies DR, Proc Natl Acad Sci U S A 2005 102 10976 10980 10.1073/pnas.0505077102 16043704 (Pubitemid 41105978)
13. Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Xu Y, Tao X, Shen B, Horng T, Medzhitov R, Manley JL, Tong L, Nature 2000 408 111 115 10.1038/35040600 11081518
14. Sequence variability and protein domain architectures for bovine Toll-like receptors 1, 5, and 10. Seabury CM, Cargill EJ, Womack JE, Genomics 2007 90 502 515 10.1016/j.ygeno.2007.07.001 17719743 (Pubitemid 47404803)
15. Evolution of the bovine TLR gene family and member associations with Mycobacterium avium subspecies paratuberculosis infection. Fisher CA, Bhattarai EK, Osterstock JB, Dowd SE, Seabury PM, Vikram M, Whitlock RH, Schukken YH, Schnabel RD, Taylor JF, et al. PLoS One 2011 6 27744 10.1371/journal.pone. 0027744 22164200
16. The role of positive selection in determining the molecular cause of species differences in disease. Vamathevan JJ, Hasan S, Emes RD, Amrine-Madsen H, Rajagopalan D, Topp SD, Kumar V, Word M, Simmons MD, Foord SM, et al. BMC Evol Biol 2008 8 273 10.1186/1471-2148-8-273 18837980
17. Molecular evolution of bovine Toll-like receptor 2 suggests substitutions of functional relevance. Jann OC, Werling D, Chang JS, Haig D, Glass EJ, BMC Evol Biol 2008 8 288 10.1186/1471-2148-8-288 18937834
18. Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Gibbs RA, Taylor JF, Van Tassell CP, Barendse W, Eversole KA, Gill CA, Green RD, Hamernik DL, Kappes SM, Lien S, et al. Science 2009 324 528 532 19390050
19. The structure of the TLR5-flagellin complex: a new mode of pathogen detection, conserved receptor dimerization for signaling. Lu J, Sun PD, Sci Signal 2012 5 e11 10.1126/scisignal.2002963 22720339
20. Structural basis of TLR5-flagellin recognition and signaling. Yoon SI, Kurnasov O, Natarajan V, Hong M, Gudkov AV, Osterman AL, Wilson IA, Science 2012 335 859 864 10.1126/science.1215584 22344444
21. Flagellin expression enhances Salmonella accumulation in TLR5-positive macrophages. Metcalfe HJ, Best A, Kanellos T, La Ragione RM, Werling D, Dev Comp Immunol 2010 34 797 804 10.1016/j.dci.2010.02.008 20188752
22. Identification of conserved domains in Salmonella muenchen flagellin that are essential for its ability to activate TLR5 and to induce an inflammatory response in vitro. Murthy KG, Deb A, Goonesekera S, Szabo C, Salzman AL, J Biol Chem 2004 279 5667 5675 14634022 (Pubitemid 38220595)
23. Two modes of ligand recognition by TLRs. Brodsky I, Medzhitov R, Cell 2007 130 979 981 10.1016/j.cell.2007.09.009 17889640 (Pubitemid 47410282)
24. Effects of single nucleotide polymorphisms on Toll-like receptor 3 activity and expression in cultured cells. Ranjith-Kumar CT, Miller W, Sun J, Xiong J, Santos J, Yarbrough I, Lamb RJ, Mills J, Duffy KE, Hoose S, et al. J Biol Chem 2007 282 17696 17705 10.1074/jbc.M700209200 17434873 (Pubitemid 47100325)
25. A common human TLR1 polymorphism regulates the innate immune response to lipopeptides. Hawn TR, Misch EA, Dunstan SJ, Thwaites GE, Lan NT, Quy HT, Chau TT, Rodrigues S, Nachman A, Janer M, et al. Eur J Immunol 2007 37 2280 2289 10.1002/eji.200737034 17595679 (Pubitemid 47250219)
26. Diversity and evolution of 11 innate immune genes in Bos taurus taurus and Bos taurus indicus cattle. Seabury CM, Seabury PM, Decker JE, Schnabel RD, Taylor JF, Womack JE, Proc Natl Acad Sci U S A 2010 107 151 156 10.1073/pnas.0913006107 20018671
27. SIFT: Predicting amino acid changes that affect protein function. Ng PC, Henikoff S, Nucleic Acids Res 2003 31 3812 3814 10.1093/nar/gkg509 12824425 (Pubitemid 37442253)
28. The crystal structure of the human toll-like receptor 10 cytoplasmic domain reveals a putative signaling dimer. Nyman T, Stenmark P, Flodin S, Johansson I, Hammarstrom M, Nordlund P, J Biol Chem 2008 283 11861 11865 10.1074/jbc.C800001200 18332149
29. Extensive protein and microsatellite variability in an isolated, cyclic ungulate population. Bancroft DR, Pemberton JM, King P, Heredity (Edinb) 1995 74 Pt 3 326 336
30. Evidence for two independent domestications of cattle. Loftus RT, MacHugh DE, Bradley DG, Sharp PM, Cunningham P, Proc Natl Acad Sci U S A 1994 91 2757 2761 10.1073/pnas.91.7.2757 8146187 (Pubitemid 24139427)
31. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. Edgar RC, BMC Bioinforma 2004 5 113 10.1186/1471-2105-5-113 (Pubitemid 40195393)
32. Molecular phylogenetics and the origins of placental mammals. Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ, Nature 2001 409 614 618 10.1038/35054550 11214319 (Pubitemid 32154812)
33. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Nielsen R, Yang Z, Genetics 1998 148 929 936 9539414 (Pubitemid 28169008)
34. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Wong WS, Yang Z, Goldman N, Nielsen R, Genetics 2004 168 1041 1051 10.1534/genetics.104.031153 15514074 (Pubitemid 39491478)
35. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Yang Z, Nielsen R, Goldman N, Pedersen AM, Genetics 2000 155 431 449 10790415 (Pubitemid 30257141)
36. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Zhang J, Nielsen R, Yang Z, Mol Biol Evol 2005 22 2472 2479 10.1093/molbev/msi237 16107592 (Pubitemid 41661383)
37. Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD, Mol Biol Evol 2008 25 207 219 18032407
38. A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. Bielawski JP, Yang Z, J Mol Evol 2004 59 121 132 15383915 (Pubitemid 38858437)
39. An Improved Likelihood Ratio Test for Detecting Site-Specific Functional Divergence among Clades of Protein-Coding Genes. Weadick CJ, Chang BS, Mol Biol Evol 2012 29 1297 1300 10.1093/molbev/msr311 22319160
40. False-positive results obtained from the branch-site test of positive selection. Suzuki Y, Genes Genet Syst 2008 83 331 338 10.1266/ggs.83.331 18931458
41. Simple solution to a common statistical problem: interpreting multiple tests. Gordi T, Khamis H, Clin Ther 2004 26 780 786 10.1016/S0149-2918(04)90078- 1 15220022 (Pubitemid 38736968)
42. Bayes empirical bayes inference of amino acid sites under positive selection. Yang Z, Wong WS, Nielsen R, Mol Biol Evol 2005 22 1107 1118 10.1093/molbev/msi097 15689528 (Pubitemid 40471423)
43. Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Nozawa M, Suzuki Y, Nei M, Proc Natl Acad Sci U S A 2009 106 6700 6705 10.1073/pnas.0901855106 19339501
44. Statistical properties of the branch-site test of positive selection. Yang Z, dos Reis M, Mol Biol Evol 2011 28 1217 1228 10.1093/molbev/msq303 21087944
45. In defense of statistical methods for detecting positive selection. Yang Z, Nielsen R, Goldman N, Proc Natl Acad Sci U S A 2009 106 95 author reply E96 10.1073/pnas.0904550106 19805241
46. LRRfinder: a web application for the identification of leucine-rich repeats and an integrative Toll-like receptor database. Offord V, Coffey TJ, Werling D, Dev Comp Immunol 2010 34 1035 1041 10.1016/j.dci.2010.05.004 20470819
47. SMART 6: recent updates and new developments. Letunic I, Doerks T, Bork P, Nucleic Acids Res 2009 37 229 D232 10.1093/nar/gkn808 18978020
48. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Krogh A, Larsson B, von Heijne G, Sonnhammer EL, J Mol Biol 2001 305 567 580 10.1006/jmbi.2000.4315 11152613 (Pubitemid 33032862)
49. The PSIPRED protein structure prediction server. McGuffin LJ, Bryson K, Jones DT, Bioinformatics 2000 16 404 405 10.1093/bioinformatics/16.4.404 10869041 (Pubitemid 30417087)
50. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Arnold K, Bordoli L, Kopp J, Schwede T, Bioinformatics 2006 22 195 201 10.1093/bioinformatics/bti770 16301204 (Pubitemid 43205406)
51. Disseminating structural genomics data to the public: from a data dump to an animated story. Abagyan R, Lee WH, Raush E, Budagyan L, Totrov M, Sundstrom M, Marsden BD, Trends Biochem Sci 2006 31 76 78 10.1016/j.tibs.2005.12.006 16406633 (Pubitemid 43221839)
52. The Staden sequence analysis package. Staden R, Mol Biotechnol 1996 5 233 241 10.1007/BF02900361 8837029 (Pubitemid 126441504)
53. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Tamura K, Dudley J, Nei M, Kumar S, Mol Biol Evol 2007 24 1596 1599 10.1093/molbev/msm092 17488738 (Pubitemid 47236692)